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Title Redescription and Taxonomic Reassessment of Nemertellina minuta Friedrich, 1935, sensu Yamaoka, 1940 (Nemertea,Hoplonemertea, Monostilifera)

Author(s) Kajihara, Hiroshi; Gibson, Ray; Mawatari, Shunsuke F.

Citation Zoological Science, 17(2), 265-276

Issue Date 2000-03

Doc URL http://hdl.handle.net/2115/32937

Rights (c) 日本動物学会 / 本文献の公開は著者の意思に基づくものである

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ZOOLOGICAL SCIENCE 17: 265–276 (2000) © 2000 Zoological Society of Japan

* Corresponding author: Tel. +81-11-706-3524;FAX. +81-11-746-0862.

Redescription and Taxonomic Reassessment of Nemertellinaminuta Friedrich, 1935, sensu Yamaoka, 1940 (Nemertea,

Hoplonemertea, Monostilifera)

Hiroshi Kajihara1*, Ray Gibson2 and Shunsuke F. Mawatari1

1Division of Biological Sciences, Graduate School of Science, Hokkaido University,Sapporo 060-0810, Japan

2School of Biological and Earth Sciences, Liverpool John Moores University,Byrom Street, Liverpool L3 3AF, U.K.

ABSTRACT—Nemertellina minuta Friedrich, 1935, sensu Yamaoka, 1940, from Akkeshi Bay, Japan, is fullyredescribed as a new species, Nemertellina yamaokai. The main characters distinguishing this taxon from N.minuta are the presence of two pairs of cephalic furrows and cephalic glands, and the absence of dorsoven-tral muscles from the intestinal region.

INTRODUCTION

The monostiliferous hoplonemertean genus Nemertellinawas established by Friedrich (1935a) for two species that hedescribed from Kiel Bay, Germany, Nemertellina caneaFriedrich, 1935, and N. oculata Friedrich, 1935. In the sameyear Friedrich (1935b) described a third species, N. minutaFriedrich, 1935. The fourth species, N. tropica Kirsteuer, 1965,was subsequently described by Kirsteuer (1965) from a coralreef in Madagascar. There are no other records of Nemertellinaspecies except for that of Yamaoka (1940), who reported asingle specimen, identified as N. minuta, from “the canal of [a]sponge, collected from several metres depth in Akkeshi Bay”(Yamaoka, 1940: 240). He noted that the internal structure ofthe specimen “was not clearly observed” but that the individualappeared to be referable to N. minuta because of its small,slender white body, head with a rounded anterior margin, twopairs of eyes widely separated from each other, rhynchocoelrestricted to the anterior region of the body, and conical styletbasis almost equal in length to that of the central stylet. Iwata’s(1954) reference to N. minuta occurring in Japanese waterswas based upon Yamaoka’s (1940) record, of which Gibson(1995: 427) commented that “the validity of this occurrence isuncertain.”

During 1997 and 1998 several specimens of a nemerteanwere collected from the same location in Akkeshi Bay asYamaoka’s (1940) original material. Their external appear-ance was identical to the species illustrated by Yamaoka (1940:text-fig. 15) as N. minuta. Histological studies of the anatomyof the present specimens confirm that they belong in thegenus Nemertellina.

MATERIALS AND METHODS

The nemerteans were obtained from 6-8 m depth at two sitesdredged in Akkeshi Bay, Japan, at 43°00'N, 144°46'E and 43°42'N,144 °51’E. Dredgings were made on 9 July 1997, 15 April 1998 and8-9 July 1998, all the samples comprising a mixture of bivalve mol-luscs (Patinopecten sp. and oysters), sponges, seaweeds and rocks.Each sample was placed in a container in the laboratory, coveredwith clean sea water and allowed to stand without aeration. Nemerte-ans emerging from the samples were removed over a 48-hr period, atotal of 35 individuals being obtained from all the samples. Speci-mens for histological examination were anaesthetized in 7.5% MgCl2,fixed in Bouin’s solution for 24 hr, embedded in 56–57°C m.p. paraf-fin wax and sectioned at 5–6 µm before being stained with the Mallorytrichrome method. A total of 12 specimens has been sectioned, 9transversely and 3 longitudinally. Observations on the stylet appara-tus of 32 specimens were made by the squeezing method describedby Kirsteuer (1967).

Type material is deposited in the Zoological Institute, HokkaidoUniversity, Japan(ZIHU) and the National Museum of Natural His-tory, Smithsonian Institution, Washington, D.C., U.S.A. (USNM).

RESULTS

DESCRIPTION

Family Tetrastemmatidae Hubrecht, 1879Genus Nemertellina Friedrich, 1935

Diagnosis: Friedrich (1935a) gave the following characters asdiagnostic for the genus: tip of head with both circular andlongitudinal musculature; four eyes; cerebral organs simple,not extending back to pre-cerebral septum, opening by poresnear the anterior pair of eyes; no cephalic furrows; pre-cere-bral septum closed but differently formed in the different spe-cies; rhynchocoel not extending into posterior third of body; atransverse muscle septum present in the body which is formed

H. Kajihara et al.266

from the rhynchocoel circular muscle layer and constricts theintestine; intestine with shallow lateral diverticula; dorsoven-tral muscles weakly developed.

Friedrich’s (1936) generic diagnosis for the genus wasessentially the same, although he made no mention of theeye number. Kirsteuer (1965) noted that important anatomi-cal features diagnostic of the genus Nemertellina included theposition of the cerebral sensory organs in the tip of the head,a closed pre-cerebral septum, a short rhynchocoel reachingto between 50 and 66% of the body length, a single intestinalcaecum, lateral nerve cords with a single neuropil, and a com-pact transverse septum in the vicinity of the caudal end of therhynchocoel formed from the circular muscle fibres of therhynchocoel wall. With the exception of rhynchocoel lengthand eye number, none of these features was recorded byYamaoka.

Nemertellina yamaokai sp. nov.(Figs 1–33)

Synonyms : Nemertellina minuta Yamaoka, 1940: 239–240,text-figs 15, 16; Iwata, 1954: 2, 15, Table 1.Etymology : The species is named after Teiichi Yamaoka, bothas a tribute to his work on the nemertean fauna of Japan andas the original finder of the present species.Type specimens : Type specimens consist of the holotype,immature male, complete series of transverse sections, 26slides (ZIHU-01260) and paratypes, female, series of trans-verse sections, 24 slides (ZIHU-01261), male, completeseries of longitudinal sections, 14 slides (ZIHU-01262) andfemale, complete series of transverse sections, 17 slides(USNM 186063). Three unsectioned voucher specimens arealso deposited under ZIHU-1271, ZIHU-1272 and ZIHU-1273.Type locality : Akkeshi Bay, Japan, 6-8 m depth amongsponges, seaweeds, rocks and molluscs (Patinopecten sp.and oysters), 43°00'N, 144°46'E.Other locations : Akkeshi Bay, Japan, 43°42'N, 144°51'E, simi-lar depth and substrate to the type locality; Akkeshi Bay, inthe canal of a sponge from several metres depth (Yamaoka,1940).External features : The body is slender, filiform and with analmost uniform width throughout its length (Figs 1, 2); speci-mens were from 7–30 mm long and 250–625 µm in diameter(Table 1). There is no distinct colour pattern, the anteriorregion being white, the intestinal region variously pure whiteto pale yellow. The cerebral ganglia are usually distinguish-able by their reddish coloration. The anteriorly rounded headis not wider than the adjacent body, the posterior end is slightlypointed. The four distinct eyes are arranged to form the cor-ners of an elongate rectangle (Fig. 1A). There are two pairs ofcephalic furrows (Fig. 1), one pair behind each pair of eyes.The anterior furrows curve forward on the ventral surface,meeting to form a longitudinal median groove that extendstowards the tip of the head (Fig. 1B), the posterior furrowscompletely encircle the head, forming a posteriorly directedV-shape on its dorsal surface (Fig. 1A). Approximately one-third of the distance along the body there is a distinct epider-

mal constriction (Figs 1–3), situated just in front of the poste-rior end of the rhynchocoel.

Body wall, musculature and parenchyma: The ciliated andglandular epidermis (Fig. 4) is 12–30 µm thick, but with fewacidophilic gland cells in the ventral pre-cerebral regions ofthe head (Figs 4–7) compared with other regions of the body.Basally the epidermis possesses a distinct basal-cup zone,as described by Norenburg (1985). The dermis is only 1–7µm thick but distinct (Fig. 8). The body wall musculature ismost strongly developed in the foregut region; the circularmuscle layer (Fig. 8), extending the full length of the body,has a maximum thickness of 5–6 µm but is mostly less thanthis, while the longitudinal musculature (Fig. 8) is 10–30 µmdeep in the anterior regions but caudally reduced to only 5–7µm. The longitudinal layer is not anteriorly divided, as in sev-eral monostiliferous genera, most of its fibres pre-cerebrallyturning inwards to form the proboscis insertion (Fig. 7),although isolated fibres or fibre bundles continue anteriorlyas the cephalic retractor muscles.

Throughout the cephalic region many of the longitudinalfibres turn inwards to contribute to a loose meshwork of fibreswhich extends between the cephalic glands surrounding therhynchodaeum (Fig. 4). There is no diagonal muscle layer inthe body wall, nor was evidence of dorsoventral musclebundles found in any part of the body.

Parenchymatous connective tissues are but sparinglydeveloped throughout the body.Proboscis apparatus : The subterminal, ventral proboscis poreopens from the longitudinal median groove formed by theanterior pair of cephalic furrows. The rhynchodaeal epithe-lium is delicate, mostly 2–5 µm thick but reaching a depth ofabout 10 µm just in front of the proboscis insertion (Figs 4, 9–11), but neither ciliated nor glandular. There is no rhynchodaealsphincter.

The rhynchocoel is between 30–60% of the body length.Its wall contains separate circular and longitudinal muscle lay-ers, each mostly only one or two fibres thick. In that portion ofthe body where the proboscis retractor muscle is attached tothe rhynchocoel wall the circular muscle layer is dissolved toform an intestinal sphincter (Figs 12, 13), corresponding inposition to the epidermal annular constriction.

The proboscis, slightly longer than the rhynchocoel, pos-sesses a typical monostiliferous construction as described byGibson (1972). The most anterior portion of the proboscis,leading from the proboscis insertion, is short, only 35–50 µmin diameter and composed only of a longitudinal muscle layerabout 15 µm in maximum thickness flanked on its inner andouter surfaces by a thin connective tissue lining. The mainanterior region (Fig. 14) in the retracted position, however, is45-60% of the overall body diameter and comprises a papil-late epithelium 40–70 µm tall, a connective tissue basementlayer, a delicate outer circular muscle layer only 2–3 fibresthick, an inner longitudinal muscle coat 7–20 µm across, adelicate inner connective tissue membrane and a flattenedinner lining. The 9–10 proboscis nerves are generally smalland indistinct; they run in the longitudinal muscle layer and

Redescription of Nemertellina minuta from Japan 267

Figs 1–3. Nemertellina yamaokai sp. nov. 1. Drawings to show the external features of the anterior region viewed from dorsal (A) and ventral(B) aspect. Redrawn from Yamaoka’s (1940: text-fig. 15) illustration of the specimen he identified as Nemertellina minuta. 2. Photograph of aliving specimen, viewed dorsally. The arrow indicates the position of the annular epidermal constriction. 3. Photomicrograph of the anterior bodyregion of an anaesthetized and squeezed specimen, showing the annular epidermal constriction (indicated by the arrow), cerebral ganglia,proboscis and arrangement of the eyes. The distance between anterior and posterior pairs of eyes compared to that observed in freely movingindividuals is decreased as a consequence of contraction. Scale bars=1 mm.


are peripherally linked by delicate interneural connectives (Fig.14).

The stylet bulb region (Figs 15, 16) conforms to thegeneralised monostiliferous condition described by Gibson(1972). The central stylet (Fig. 17) is smooth and 37–63 µmlong (Table 1), its basis 43–65 µm long and with a taperedcylindrical shape. The stylet : basis ratio varies from 1 : 0.86to 1 : 1.43 with an average value of 1 : 1.08. In most individu-als there are two accessory stylet pouches, each typicallycontaining four or five reserve stylets (range 1–7) (Fig. 16),although one individual possessed three accessory pouchesand one had four (Table 1).

The posterior portion of the proboscis (Fig. 18) is about30–40% of the body diameter; it possesses neither epithelialpapillae nor an obvious neural supply. Its outer longitudinalmuscle layer is 2–5 µm thick, whereas its inner circular musclelayer is extremely thin and poorly developed.Alimentary canal : The oesophagus (Figs 4, 19, 20) is thin-walled, 2–10 µm in diameter, and neither ciliated nor glandu-

lar. It emerges from the ventral floor of the rhynchodaeumclose in front of the proboscis insertion, leading posteriorly tomerge with the stomach behind the brain. The transitionbetween oesophagus and stomach is marked by the appear-ance of cilia and basophilic gland cells (Fig. 19). The stomach(Figs 8, 21, 23) wall is not deeply folded, its epithelium, whichis dominated by basophilic glands, decreasing in thicknessfrom an anterior height of about 50 µm commensurate with aposterior decline in the density of gland cell numbers as itapproaches the slender pyloric canal (Fig. 22).

From the junction between the pylorus and intestine ashort intestinal caecum (Fig. 23) extends anteriorly below therear half of the stomach. The caecum possesses neitheranterior nor lateral diverticula. The intestine is simple, withpaired shallow lateral pouches (Fig. 24) and opens via theanus at the extreme posterior tip of the body.Blood system : The organization of the blood system broadlyresembles the basic hoplonemertean pattern illustrated byGibson (1972: fig. 14A). The anterior cephalic loop leads to a

Table 1. The body lengths and widths, central stylet and basis lengths and number of accessory stylet pouches and their contained reservestylets recorded for 33 specimens of Nemertellina yamaokai sp. nov.

Specimen Body BodyLength of Length of Number of Numbers of

number length in mm width in µmcentral stylet stylet basis accessory stylet accessory stylets per

in µm in µm pouches pouch

1 7 250 43 43 2 4, 42 18 300 51 65 2 4, 43 14 380 53 53 ? ?4 16 400 58 59 2 6, 35 11 380 63 56 2 5, 46 16 500 59 60 2 4, 47 13 280 51 51 2 3, 38 15 350 53 49 2 3, 39 14 250 51 53 2 4, 3

10 18 380 46 48 2 3, 311 16 280 63 55 2 4, 312 20 500 61 58 2 4, 313 10 380 59 51 2 4, 414 30 625 59 59 2 4, 315 8 500 45 53 2 4, 416 10 450 53 48 2 7, 517 14 375 42 54 2 4, 318 13 375 A A 2 1, 219 10 450 37 53 2 4, 520 13 375 49 53 2 4, 321 20 500 51 64 2 4, 422 12 500 53 57 2 4, 523 12 375 49 55 2 4, 424 25 500 54 53 2 4, 525 17 375 53 49 2 3, 326 17 450 60 59 2 3, 327 13 375 52 58 2 4, 528 7 370 47 45 4 3, 3, 3, 229 25 625 43 60 2 3, 330 7 380 38 44 2 4, 331 15 500 50 58 3 4, 3, 332 28 450 49 61 2 4, 533 20 500 45 60 2 6, 7

Mean±S.E. 15.27±5.77 414.55±93.08 51.25±6.70 54.50±5.35 2.09±0.38 3.78±1.04

? = not recordedA = missing from proboscis


pair of cephalic vessels which at first flank the rhynchodaeumas they run posteriorly (Figs 9–10), but farther back comeinto close contact with the medial parts of the posterior regionof the cerebral sensory organs (Figs 4, 11). As they passthrough the cerebral ring the vessels protrude into therhynchocoel (Fig. 19) to form a pair of thin-walled and flat-tened vascular plugs. Post-cerebrally the vessels continueback close to the lateral nerve cords, meeting near the tail bya supraintestinal connective. The origin of the mid-dorsal bloodvessel is unusually far back, behind the brain region; it emergesas a branch from one of the lateral vessels between the ante-rior and posterior stomach regions of the body to extend pos-teriorly close to the ventral rhynchocoel wall (Fig. 12) or,behind the end of the rhynchocoel, above the intestine (Fig.24). At its posterior end the mid-dorsal vessel joins thesupraintestinal connective. There are no pseudometamerictransverse connectives between the three longitudinal ves-sels in any part of the body.Nervous system : The moderately large cerebral ganglia aretransversely linked by a thin (6–10 µm) dorsal commissureand thicker (17–40 µm) ventral commissure, the former situ-ated somewhat in front of or directly above the latter. Theganglia are enclosed by a thin but distinct outer neurilemma,but there is no inner neurilemma between the fibrous and

ganglionic components of the brain. The lateral nerve cordscontain one or two myofibrillae (Fig. 25), but possess neitheraccessory nerves nor neurochords. The lateral nerves meetposteriorly by a supraintestinal commissure.

Several cephalic nerves extend from the anterior and lat-eral margins of each cerebral lobe. One pair of nerves fromthe dorsal ganglia connect to the cerebral sensory organs,others appear to lead to the eyes and proboscis. From eachventral lobe a distinct lateroventral nerve emerges justbehind the ventral commissure, passes through the outer neu-rilemma and continues posteriorly alongside the brain to theanterior stomach region, where it turns ventrally towards thestomach wall; these two nerves apparently innervate the stom-ach but their ultimate fate could not be traced. There is nomid-dorsal nerve.Excretory system : The excretory system is mainly located oneither side of the rhynchocoel (Figs 8, 23), extending from theposterior region of the stomach forwards to the lateral mar-gins of the brain. The collecting tubules have a maximumdiameter of about 25 µm and possess thick walls, up to 12 µmacross. Near their anterior limits the tubule on each side ofthe body leads to an efferent duct which turns ventrolaterallyto open by a single nephridiopore about 10 µm in diameter;the position of the nephridiopores appears to depend upon

Figs 4–7. Nemertellina yamaokai sp. nov. 4. Transverse section through a posterior eye (oc); note the head retractor muscle fibres indicated byan arrow running through the basophilic cephalic glands (bg). 5. Transverse section through the tip of the head to show the apical organ (ao). 6.Transverse section through the anterior pair of eyes. 7. Transverse section through the proboscis insertion. ag=acidophilic gland cells; cv=cephalicblood vessel; ep=epidermis; oe=oesophagus; pc=posterior portion of cerebral organ; rd=rhynchodaeum. Scale bars: 4–6=50 µm; 7=100 µm


Figs 8–13. Nemertellina yamaokai sp. nov. 8. Transverse section through the stomach (st) region to show the lateral position of the excretorycollecting tubules (ex). 9. Transverse section through the anterior portion of a cerebral organ, showing a ciliated cerebral canal (cc) indicated bythe larger arrow. A cephalic blood vessel (cv) is indicated by the smaller arrow. 10. Transverse section through the narrowed ‘neck’ (nn)connecting the anterior and posterior regions of a cerebral organ. A cephalic blood vessel (cv) is arrowed. 11. Transverse section through theposterior portion (pc) of a cerebral organ to show its close association with a cephalic blood vessel (cv), indicated by an arrow. 12. Transversesection at the level of the epidermal annular constriction of one of the paratypes to show the sphincter (is) formed by the circular muscle layer ofthe rhynchocoel wall and the constricted portion of the intestine (in) where it passes through this sphincter. The arrow indicates the mid-dorsalblood vessel. 13. Longitudinal section through the intestinal sphincter, arrowed, of another paratype. cm=body wall circular muscle layer;de=dermis; lm=body wall longitudinal muscle layer; ln=lateral nerve cord; pr=proboscis; rd=rhynchodaeum; rm=proboscis retractor muscle.Scale bars: 8, 12, 13=100 µm; 9–11=40 µm.


Figs 14–17. Nemertellina yamaokai sp. nov. 14. Transverse section through the main anterior portion of the proboscis; the 9 proboscis nervesare indicated by arrows. 15. Transverse section through the stylet bulb region of the proboscis showing the two accessory stylet pouches (ap).16. Photomicrograph of the proboscis stylet bulb region of a living individual. 17. Nomarski differential interference contrast photomicrograph ofa typical central stylet and basis, taken in a living specimen. cp=circular muscle layer of proboscis; lp=longitudinal muscle layer of proboscis;pe=proboscis epithelium. Scale bars: 14, 17=50 µm; 15, 16=100 µm.

the degree of body contraction but is located between theposterior brain (Fig. 26) and anterior stomach regions.Apical organ and cephalic glands : The single apical or frontalorgan opens close in front of the proboscis pore. It comprisesa ciliated pit, 15–60 µm in diameter, lined by an epithelium5–25 µm thick which completely lacks gland cells (Fig. 5).The cephalic glands discharge to the exterior through the api-cal organ. The typical, basophilic, vacuolate cephalic glandsextend back to the proboscis insertion, occasionally beyondthis to reach the anterior brain regions (Figs 7, 26). The glandsmainly form two compact elongate masses, one mid-dorsaland the other mid-ventral (Fig. 7). The ventral mass often in-completely encloses the oesophagus above it, and usuallyextends farther back than the dorsal mass (Fig. 27).Ocelli : There are four well-developed pigment cup ocelli, eachapproximately 25–50 µm in diameter. The anterior pair is situ-ated close to the tip of the head, the posterior pair just in frontof the proboscis insertion (Figs 4, 5).Cerebral organs : Each of the two cerebral organs opens by aventrolateral ciliated canal, 15–20 µm in diameter, which leadsinwards from the anterior cephalic furrows (Fig. 28). Theorgans possess a simple construction and an elongate hour-glass shape, forming anterior and posterior lobes which are

medially joined by a narrower ‘neck’ (Figs 28–31). The cili-ated canals terminate in a chamber medially flanked by glandcells in the anterior lobe. The anterior lobe is about 50 µm indiameter. Behind this the ‘neck’, consisting mainly ofneuroganglionic tissues but with a few gland cells interspersedbetween them, is only 5–12 µm wide (Fig. 10), whereas theposterior lobe, containing both glandular and neural compo-nents, is about 45 µm in maximum diameter. The cerebralorgan nerve leads directly from the posterior end of eachcerebral organ.Reproductive system : The sexes are separate. The sphericalgonads are restricted to the intestinal region of the body, form-ing a row on each side and broadly alternating with the lateralintestinal pouches. Mature specimens, with their gonads con-taining either ova or spermatids (Figs 32, 33), were collectedin July. The gonopores open laterodorsally above the lateralnerve cords.

SYSTEMATIC DISCUSSION

Yamaoka (1940) gave only a brief description of the singleindividual he identified as Nemertellina minuta, commenting(p. 240) that the “specimen seems to be referable to [this spe-


cies] by the following features; (1) the body is very small andslender, and is white in colour, and the head is rounded in thefrontal margin, (2) two pairs of ocelli are separated by a longdistance from each other, (3) the proboscis sheath extendsonly to the anterior region of the body, and (4) the basis ofcentral stylet is conical, with the length almost equal to that ofthe stylet.” The present material, collected from the samelocality that Yamaoka obtained his specimen, possesses allof the above features and, in external appearance, is virtuallyidentical to that illustrated by Yamaoka (1940: text-fig. 15A,B), including the presence of two pairs of cephalic furrows.The only known difference between our examples andYamaoka’s specimen is the body length; the longest of thepresent individuals measured was 30 mm, whereasYamaoka’s specimen had a length of 50 mm (misprinted as“50 mm wide” in Yamaoka, 1940: 239). Although his originalmaterial, “cut into pieces in the fixiative” (ibid., p. 240), waslost, the close similarity between Yamaoka’s and our speci-mens, especially as they came from the same location, fullyjustify them being regarded as conspecific.

Yamaoka’s (1940: 239, text-fig. 15A, B) account andillustrations of the external features of his specimen are, how-ever, at variance with Friedrich’s (1935a, 1936, 1955) genericdiagnosis of Nemertellina in that both it and the present mate-

Figs 18–21. Nemertellina yamaokai sp. nov. 18. Transverse section through the posterior region of the proboscis. 19. Transverse sectionthrough the posterior brain region to show the two protrusions of the cephalic blood vessels, indicated by arrows, into the rhynchocoel wall. 20.Transverse section through the ventral cerebral commissure (vc). 21. Transverse section through the stomach (st). oe=oesophagus; pr=proboscis;rc=rhynchocoel; vg=ventral cerebral ganglion. Scale bars: 18=100 µm; 19–21=50 µm.

rial possess two pairs of cephalic furrows, whereas N. canea,N. minuta and N. oculata completely lack cephalic furrows.Kirsteuer (1965) makes no reference to the presence of cepha-lic furrows in his description of the external features of N.tropica, referring to the cerebral organs (p. 305) as opening“mit einem ventrolateralen Porus, welcher sich am oberenEnde einer histologisch nicht als Kopffurche gekennzeichnetenEintellung befindet.” The presence of two pairs of cephalicfurrows in both Yamaoka’s and the present specimens thusprecludes them from being identifiable with N. minuta or withany of the other known members of the genus.

Table 2 summarises the major anatomical features of thepresent specimens compared with those described for the fourpreviously known species of Nemertellina, and there is littledoubt that the Japanese taxon should be included in thisgenus, particularly by the nature and position of its cerebralorgans, possession of a closed pre-cerebral septum and shortrhynchocoel, by the general organization of its alimentarycanal with a short intestinal caecum and shallow lateral intes-tinal pouches and, especially, by the presence of its mid-bodytransverse muscular septum which forms a constriction aroundthe intestine. On the basis of these similarities we believe thatit would be unjustifiable to exclude the Japanese specimensfrom the genus Nemertellina merely on the grounds that they


Figs 22–27. Nemertellina yamaokai sp. nov. 22. Transverse section through the pyloric portion (py) of the foregut. 23. Transverse sectionthrough the intestinal caecum (ic). 24. Transverse section through the intestine (in) of the holotype to show the distribution of the immaturegonads (go). Mid-dorsal (dv) and lateral (lv) blood vessels are indicated by arrows. 25. Transverse section through a lateral nerve cord in theintestinal region; the arrow indicates a myofibrilla. 26. Transverse section through the posterior brain region to show a ventrolateral nephridiopore(np). 27. Transverse section through the brain region at the level of the dorsal cerebral commissure (dc). bg=basophilic cephalic glands;dg=dorsal cerebral ganglion; ln=lateral nerve cord; oe=oesophagus; pr=proboscis. Scale bars: 22, 23, 27=100 µm; 24, 26=50 µm; 25=10 µm.


possess cephalic furrows whereas other species do not; othermonostiliferous genera are known, for example Tetrastemma,in which different species may possess two, one or no pairsof cephalic furrows (Gibson, 1994).

Several of the morphological features described for thepresent species cannot be compared with those of the previ-ously known taxa; for example none of Friedrich’s descrip-tions gives any information on the arrangement of the bloodsystem, and Kirsteuer (1965) merely notes that in N. tropicathe mid-dorsal vessel arises by branching off the left lateralvessel and does not enter the rhynchocoel wall. Neverthe-less, the Japanese species can be distinguished from all theother known members of the genus Nemertellina by the fol-

Figs 28–33. Nemertellina yamaokai sp. nov. 28–31. Serial longitudinal sections through the pre-cerebral region to show the ciliated cerebralcanal (cc), anterior (ac) and posterior (pc) portions of a cerebral organ and the narrowed ‘neck’ (nn) which connects them. The arrowhead in Fig.28 indicates an anterior cephalic furrow, the arrow a longitudinal muscle fibre. 32. Transverse section through the intestinal region of a maturefemale paratype to show the position of the ovaries (ov). 33. Transverse section to show a testis (ts) in a mature male paratype. dg=dorsalcerebral ganglion; dv=mid-dorsal blood vessel; ln=lateral nerve cord; lv=lateral blood vessel. Scale bars: 28–32=100 µm; 33=50 µm.

lowing characters: from all four species by its possession ofcephalic furrows; from N. minuta by its possession of cephalicglands and lack of dorsoventral musculature in the intestinalregion; from N. oculata by having no median dorsal nerve norposterior rhynchodaeal sac; and from N. tropica by possess-ing only two muscle layers in the wall of the main anteriorproboscis chamber and in lacking the dorsal appendix devel-opment at the junction between foregut and intestine. Thespecies from Akkeshi Bay is accordingly redescribed aboveas Nemertellina yamaokai sp. nov.

In the light of the present studies a revised diagnosis forthe genus Nemertellina is provided:Diagnosis: Monostiliferous marine hoplonemerteans;


Table 2. Anatomical characters of the present nemerteans from Japan compared with those of the four previously described species ofNemertellina. Data obtained from Friedrich (1935a, b), Kirsteuer (1965) and the present studies.

Character N. canea N. minuta N. oculata N. tropica Present species

A. Features shared by all five taxa

Tip of head containing bothcircular and longitudinal body + + + + +wall muscle layers

Cerebral organs small, simple,situated far anterior to brain + + + + +lobes and opening near the tip ofthe head

Rhynchocoel not extending intoposterior third of body + + + + +

Rhynchocoel wall containingseparate circular and longitudinal + + + + +muscle layers

Transverse muscle septum formedfrom rhynchocoel wall circularmusculature present in intestinal + + + + +region and forming constrictionaround intestine

Intestine with single anterior caecumwhich does not reach forwards to the + + + + +brain and lacks anterior pouches

Lateral intestinal diverticula present,shallow + + + + +

Lateral nerve cords with single fibrecore, without accessory nerves + + + + +

Gonads located in intestinal region,arranged as a single longitudinal row + + + + +on each side of the body

Eyes four, anterior and posterior + + + + +pairs widely separated

Pre-cerebral septum closed + + + + +

B. Features which can be used todistinguish between the taxa

Cephalic furrows present (+) orabsent (0) 0 0 0 0 +

Cephalic glands present (+) orabsent (0) + 0 + + +

Number of proboscis nerves ? 8 ? 9 9–10

Length of rhynchocoel as a %of the body 50–60? 50 60 50 30–60

Short dorsal nerve present (+)or absent (0) 0? 0? + 0 0

Number of muscle layers in wallof main anterior proboscis chamber ? ? ? 3 2

Number of accessory stylet pouchesin stylet bulb region of proboscis 2 2 2 2 2–4

Junction of foregut and intestinewith (+) or without (0) posteriorly ? ? ? + 0directed dorsal foregut appendix

Weakly developed dorsoventralmuscles present (+) or absent (0) + + 0 ? 0in intestinal region

Rhynchodaeum at rear extendingbelow anterior part of rhynchocoel 0 0 + 0 0as a short blind-ending sac


rhynchocoel between 30 and 66% of body length, with wallcontaining separate circular and longitudinal muscle layers;transverse muscle septum which forms a constriction aroundintestine developed from circular muscle layer of rhynchocoelwall; proboscis armature consisting of single central stylet and2–4 accessory stylet pouches; body wall musculature withoutdiagonal layer, longitudinal muscles not divided anteriorly; pre-cerebral septum closed; tip of head with both circular and lon-gitudinal body wall muscle layers; cephalic glands present orabsent; cerebral organs small and simple, situated far ante-rior to the brain and opening near the tip of the head; lateralnerve cords with single fibre core, without accessory nerves;intestine with single anterior caecum which does not reachthe brain and lacks anterior pouches, intestine with shallowlateral diverticula; blood system simple, with three post-cerebral longitudinal vessels which are not linked bypseudometameric transverse connectives; four eyes, anteriorand posterior pairs widely separated; sexes separate, gonadsarranged in single longitudinal row on either side of the intes-tine; cephalic furrows present or absent.

ACKNOWLEDGEMENTS

We are grateful to Dr H. Mukai, Director of the Akkeshi MarineBiological Station, Hokkaido University, for providing the facilities forour research. We gratefully acknowledge the help of the staff of theAMBS and the kind assistance of Dr Y. Takashima, Mr T. Kato andMr M. Shimomura in obtaining specimens. We would like to express

our appreciation to Dr Janet Moore and Frank Crandall for their criti-cal reading of the original manuscript.

REFERENCES

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(Received August 30, 1999 / Accepted October 7, 1999)

redescription and taxonomic reassessment of nemertellina ......* corresponding author: tel....

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